Ciência Rural,Anatomo-pathological Santa Maria, v.47: aspects 02, e20160547, of parasitism by2017 nematodes of the superfamily http://dx.doi.org/10.1590/0103-8478cr20160547 Metastrongyloidea in wild... 1 ISSNe 1678-4596 PARASITOLOGY
Anatomo-pathological aspects of parasitism by nematodes of the superfamily Metastrongyloidea in wild crab-eating fox (Cerdocyon thous) in Midwestern Brazil
Jair Alves Ferreira Júnior1* Guilherme Reis Blume2 Susy Karoline Hermes de Sousa1 Clarissa Machado de Carvalho3 Chris Gardiner4
1Laboratório de Patologia Veterinária, Universidade de Brasília (UnB), 70910-900, Brasília, DF, Brasil. Email: [email protected]. *Corresponding author. 2Laboratório de Diagnóstico Patológico Veterinário, Universidade de Brasília (UnB), Brasília, DF, Brasil. 3Consultório Mundo Silvestre, Asa Norte, Brasília, DF, Brasil. 4Veterinary Pathology Service, Joint Pathology Center, Silver Spring, MD, USA.
ABSTRACT: Nematodes of the superfamily Metastrongyloidea affect the respiratory, cardiovascular, and nervous systems of domestic carnivores and are uncommonly detected in wild animals. This report describes the lesions associated with pulmonary parasitism by nematodes of the superfamily Metastrongyloidea in a wild crab-eating fox (Cerdocyon thous) in the Federal District, Brazil. Grossly, there was pulmonary hyperemia, edema, and emphysema. Microscopically, there was granulomatous arteritis associated with intravascular metastrongylid. The anatomical location, characteristic lesion, and histological features of the parasite suggested that the nematode involved in this case is Angiostrongylus vasorum. This worm is frequently reported parasitizing pulmonary arteries of domestic canids but is uncommonly described in wild canids in Midwestern Brazil. Key words: Angiostrongylus, nematode, wild canids, pathology.
Aspectos anatomopatológicos do parasitismo por nematódeos da superfamília Metastrongyloidea em cachorro-do-mato (Cerdocyon thous) de vida livre no Centro-Oeste brasileiro
RESUMO: Nematódeos da superfamília Metastrongyloidea afetam o sistema respiratório, cardiovascular e nervoso de carnívoros domésticos e são incomuns em animais silvestres. Este trabalho descreve os achados anatomopatológicos de um caso de parasitismo pulmonar por nematódeos da superfamília Metastrongyloidea em um cachorro-do-mato (Cerdocyon thous) de vida livre no Distrito Federal. Macroscopicamente, o pulmão apresentou hiperemia, edema e enfisema e, no exame histológico, notou-se arterite granulomatosa associada à metastrongilídeos intravasculares. A localização anatômica, o tipo de lesão observada e os aspectos histológicos do parasito sugerem que o nematódeo, envolvido neste caso, seja o Angiostrongylus vasorum, que é frequentemente descrito parasitando artérias pulmonares de canídeos domésticos, porém, é incomumente descrito em canídeos silvestres, principalmente no Centro-Oeste brasileiro. Palavras-chave: Angiostrongylus, nematódeo, canídeos silvestres, descrição anatomopatológica.
The crab-eating fox (Cerdocyon thous) is a revealed Angiostrongylus in crab-eating fox (C. thous) canid widely distributed in South America. In Brazil, (VIEIRA et al., 2008); however, the information about with the exception of the Amazon Basin, this species the morphological changes caused by these parasites is widely distributed, especially in the Midwestern is scarce. Other authors reported lesions associated region. This canid is omnivorous and eat carcasses of with this parasitism in a coyote (Canis latrans) small mammals (COURTENAY & MAFFEI, 2004). in Canada (BOURQUE et al., 2005). Our report The superfamily Metastrongyloidea is described the histopathological findings associated composed of nematodes that infect the respiratory, with the parasitism by nematodes of the superfamily cardiovascular, and nervous systems of mammals. Metastrongyloidea in a wild crab-eating fox (C. thous) This superfamily includes the Angiostrongylidae in the Federal District, Midwestern Brazil. family, which contains the genus Angiostrongylus, A free-ranging adult, female crab-eating fox with nematodes found mostly in the pulmonary (C. thous) was admitted by the government wildlife artery, its ramifications, and the right ventricle of screening center (Centro de Triagem de Animais carnivores (BOWMAN, 2010; SPRATT, 2015). A Silvestres) to the teaching veterinary hospital of parasitological review of wild carnivores in Brazil Universidade de Brasília with a history of multiple
Received 06.03.16 Approved 09.26.16 Returned by the author 11.27.16 CR-2016-0547.R1 Ciência Rural, v.47, n.2, 2017. 2 Ferreira Júnior et al. fractures. Radiographical examination revealed a al., 2007). Cases of parasitism by Angiostrongylus spp. complete vertebral fracture in the eighth thoracic in C. thous were reported in the states of Rio de Janeiro vertebra (T8). Additionally, the urine was dark red. This and Mato Grosso do Sul (TRAVASSOS & FREITAS animal was euthanized with intramuscular ketamine, 1943); whereas, A. raillieti was described in Rio de xylazine, and intracardiac potassium chloride due Janeiro (TRAVASSOS, 1927) and Goiás (VICENTE et to poor prognosis. At necropsy, samples of multiple al., 1997), and A. vasorum in Minas Gerais (DUARTE organs were collected and subsequently fixed in et al., 2007). However, detailed pathological studies of 10% buffered formalin. Tissues were processed for this infection in wild animals are extremely scarce. routine histopathological evaluation and stained with In the current report, the cause of death hematoxylin and eosin. was multiple traumas, probably due to a car accident. Grossly, mild hemoperitoneum and Although significant parasitic vascular changes in hemothorax were noted. There was a focal discrete the lung were observed, this finding was considered fibrinous adhesion of the omentum to the parietal incidental. Morphologically these parasites are peritoneum, and moderate focally extensive hemorrhage compatible with nematodes of the superfamily in the adjacent muscles, capsule, and hilum of the right Metastrongyloidea, most probably Angiostrongylus. kidney. Lungs were not collapsed and presented areas Features such as the coelomyarian-polymyarian of focally extensive emphysema in the cranial lobes musculature, accessory hypodermal chords, intestine and severe congestion in the caudal lobes (Figure 1A). with few multinucleated cells, developed the There was mild edema in the tracheal and bronchial reproductive system, and location of these parasites lumen. The mucosa of the duodenum and jejunum support this hypothesis since these characteristics are presented moderate hyperemia. The urine was mildly widely described for metastrongylids (GARDINER brownish. There was a simple and complete fracture & POYNTON, 2006). Final confirmation of this in the ventral region of the body of T8. Muscles and nematode could be made with parasitological or adjacent pleura were intensely hemorrhagic. molecular tests, such as polymerase chain reaction Microscopically, four transversal (PCR). Gross lesions characterized by poorly defined, sections of the nematodes of the superfamily scattered, slightly firm nodules in the lungs were Metastrongyloidea, measuring about 200-300µm reported in a coyote (Canis latrans) parasitized by in diameter, were observed in the lumen of the A. vasorum in Canada (BOURQUE et al., 2005). In pulmonary artery (Figure 1B). Nematodes had a the present case, gross pulmonary lesions related to pseudocoelom with smooth eosinophilic cuticle, parasites were not seen. Vascular lesions caused by coelomyarian-polymyarian musculature, accessory adult Angyostrongylus spp. occur mainly in the lung hypodermal chords, small lateral chords, an and consist of lymphoplasmacytic, eosinophilic, or intestine with few multinucleated cells (Figure 1D), granulomatous inflammation with hypertrophy of the and a developed reproductive system. Reproductive tunica intima and media (proliferative arteritis) and tract was composed of a large uterus containing a thrombosis (BOURQUE et al., 2005). In some cases, moderate amount of irregular structures, consistent it may also present as granulomatous and eosinophilic with developing eosinophilic eggs. In the wall of the pneumonia due to embolism of eggs and larvae artery, there was moderate multifocal to coalescing (CASWELL & WILLIAMS, 2015). Histological infiltration of macrophages, epithelioid cells, few findings of the current case are similar to those described lymphocytes, eosinophils, and multinucleated previously in other canids affected by this parasite; giant cells expanding to the subendothelial layer however, there was no extravasation of eggs and (Figure 1C). These findings are consistent with larvae into the interstitial space. The main differential moderate multifocal to coalescing granulomatous diagnosis for A. vasorum in canids is Dirofilaria arteritis. There were multifocal areas of moderate immitis, which also parasitizes the pulmonary arteries. atelectasis, moderate edema, and congestion. Eucoleus aerophilus, Crenosoma vulpis, Filaroides In Brazil, there are parasitological descriptions hirthi and Andersonstrongylus milksi can also affect of Angiostrongylus spp. in wild animals, such as the lungs of domestic and wild canids. However, these jaguarundi (Puma (Herpailurus) yagouaroundi) parasites only parasitize the pulmonary airways and (VIEIRA et al., 2013), hoary fox (Dusicyon vetulus) alveoli (CASWELL & WILLIAMS, 2015). (LIMA et al. 1994), montane grass mouse (Akodon Based on the histopathological findings, montensis) (SOUZA et al., 2009), and crab-eating the diagnosis of moderate multifocal to coalescing fox (C. thous) (TRAVASSOS 1927; TRAVASSOS & granulomatous arteritis associated with intralesional FREITAS 1943; VICENTE et al., 1997; DUARTE et nematodes of the superfamily Metastrongyloidea
Ciência Rural, v.47, n.2, 2017. Anatomo-pathological aspects of parasitism by nematodes of the superfamily Metastrongyloidea in wild... 3
Figure 1 - A. Cerdocyon thous. Gross appearance of the lung with areas of emphysema in the cranial lobes and congestion of the caudal lobes. B. Lung: artery with four cross-sections of intraluminal metastrongylids. Hematoxylin and eosin staining. C. Lung: granulomatous inflammation with macrophages, giant cells, lymphocytes, and rare eosinophils in the intima layer of the artery. Hematoxylin and eosin staining. D. Metastrongylid with high intestine epithelium containing few multinucleated cells (arrow). Hematoxylin and eosin staining.
was diagnosed in a wild crab-eating fox (C. thous). CASWELL, J. L.; WILLIAMS, K. J. Respiratory system. In: Anatomical location, lesion, and histological aspects MAXIE, M.G. Jubb, Kennedy, and Palmer’s pathology of domestic animals, 6. ed. St. Louis, Missouri: Saunders Elsevier, of the parasite suggest that the nematode involved 2015. V.2, Cap. 5, p. 465-591. in this case is A. vasorum, frequently described as parasitizing the pulmonary arteries of domestic COURTENAY, O.; MAFFEI, L. Crab eating fox, Cerdocyon thous canids, but it is uncommon in wild canids. This is the (Linnaeus, 1766). In: SILLERO-ZUBIRI, C. et al. Canids: foxes, wolves, jackals and dogs. Status survey and conservation action first report of this disease in wild canids in the Federal plan. Cambridge, UK: IUCN/SSC Canid Specialist Group, 2004. District, Midwestern Brazil. p. 30-38.
REFERENCES DUARTE, F. H. et al. Occurrence Angiostrongylus vasorum (Raillet, 1866) (Nematoda, Angiostrongylidae) in Cerdocyon thous Linnaeus, 1766 (Carnivora, Canidae) in Minas Gerais BOURQUE, A. et al. Angiostrongylus vasorum infection in coyote State, Brazil. Arquivo Brasileiro de Medicina Veterinária e (Canis latrans) from Newfoundlandand Labrador, Canada. Journal Zootecnia, v. 59, p. 1086-1088, 2007. Available from:
Ciência Rural, v.47, n.2, 2017. 4 Ferreira Júnior et al.
LIMA, W. S. et al. Occurrence of Angiostrongylus vasorum TRAVASSOS, L.; FREITAS, J. F. T. Relatório da sétima excursão in the lungs of the Brazilian fox Dusicyon vetulus. Journal of científica do Instituto Oswaldo Cruz, realizada a zona da Estrada Helminthology, v.68, p.87, 1994. Available from:
Ciência Rural, v.47, n.2, 2017.